Increased expression of specific recognition molecules by retinal ganglion cells and by optic pathway glia accompanies the successful regeneration of retinal axons in adult zebrafish

Journal of Comparative Neurology

Volumn 376, Issue 2, 1996, Pages 253-264

  Bernhardt, R R ^a   Tongiorgi, E ^a,b   Anzini, P ^a   Schachner, M ^a  

^a ETH ZURICH   (Switzerland)

^b SISSA   (Italy)

Author keywords

adhesion molecules; K ATPase subunit; L1; N CAM; Na; retinal development

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CELL ADHESION MOLECULE; MESSENGER RNA; NERVE CELL ADHESION MOLECULE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLIA CELL; MOLECULAR RECOGNITION; NERVE FIBER REGENERATION; NONHUMAN; OPTIC NERVE FIBER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL; ZEBRA FISH;

ANIMALS; CELL ADHESION MOLECULES; GENE EXPRESSION REGULATION; LEUKOCYTE L1 ANTIGEN COMPLEX; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; NA(+)-K(+)-EXCHANGING ATPASE; NERVE CRUSH; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEUROGLIA; OPTIC NERVE; OPTIC NERVE INJURIES; RETINAL GANGLION CELLS; RNA, MESSENGER; TENASCIN; ZEBRAFISH;

EID: 0029847135     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19961209)376:2<253::AID-CNE7>3.0.CO;2-2     Document Type: Article

References (71)

1. Aguayo, A.J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. In C. Cotman (ed): Synaptic Plasticity. New York: Guildford Press, pp. 457-484.
2. Aigner L., S. Arber, J.P. Kapfhammer, F. Botteri, H.R. Brenner, and P. Caroni (1995) Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278.
3. Antonicek, H., and M. Schachner (1988) The adhesion molecule on glia (AMOG) incorporated into lipid vesicles binds to subpopulations of neurons. J. Neurosci. 8:2961-2966.
4. Antonicek, H., E. Persohn, and M. Schachner (1987) Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration. J. Cell Biol. 104:1587-1595.
5. Appel, C., S. Gloor, G. Schmalzing, M. Schachner, and R.R. Bernhardt (in press) Expression of a Na,K-ATPase beta3 subunit during development of the zebrafish central nervous system. J. Neurosci. Res.
6. Appel, F., J. Holm, J.F. Conscience, and M. Schachner (1993) Several extracellular domains of the neural cell adhesion molecule L1 are involved in neurite outgrowth and cell body adhesion. J. Neurosci. 13:4764-4775.
7. Bähr, M., and F. Bonhoeffer (1994) Perspectives on axonal regeneration in the mammalian CNS. Trends Neurosci. 17:473-479.
8. Bartsch, S., U. Bartsch, U. Dörries, A. Faissner, A. Weller, P. Ekblom, and M. Schachner (1992) Expression of tenascin in the developing and adult cerebellar cortex. J. Neurosci. 12:736-749.
9. Bastmeyer, M., B. Schlosshauer, and C.A.O. Stuermer (1990) The spatiotemporal distribution of N-CAM in the retinotectal pathway of adult goldfish detected by monoclonal antibody D3. Development 108:299-311.
10. Bastmeyer, M., M. Beckmann, M.E. Schwab, and C.A.O. Stuermer (1991) Growth of regenerating goldfish axons is inhibited by rat oligodendrocytes and CNS myelin but not by goldfish optic nerve tract oligodendrocytelike cells and fish myelin. J. Neurosci. 11:626-640.
11. Bastmeyer, M., G. Jeserich, and C.A.O. Stuermer (1994) Similarities and differences between fish oligodendrocytes and Schwann cells in vitro. Glia 11:300-314.
12. Bastmeyer, M., H. Ott, C.A. Leppert, and C.A.O. Stuermer (1995) Fish E587 glycoprotein, a member of the L1 family of cell adhesion molecules, participates in axonal fasciculation and age-related order of ganglion cell axons in the goldfish retina. J. Cell Biol. 130:969-976
13. Battisti, W.P., J. Wang, K. Bozek, and M. Murray (1995) Macrophages, microglia, and astrocytes are rapidly activated after crush injury of the goldfish optic nerve: A light and electron microscopic analaysis. J. Comp. Neurol. 354:306-320.
14. Bernhardt, R.R. (1989) Axonal pathfinding during the regeneration of the goldfish optic pathway. J. Comp. Neurol. 284:119-134.
15. Bernhardt, R.R., A.B. Chitnis, L. Lindamer, and J.Y. Kuwada (1990) Identification of spinal neurons in the embryonic and larval zebrafish. J. Comp. Neurol. 302:603-616.
16. Berkelaar, M., D.B. Clarke, Y.C. Wang, G.M. Bray, and A.J. Aguayo (1994) Axotomy results in delayed death and apoptosis in retinal ganglon cells in adult rats. J. Neurosci. 14:4368-4374.
17. Blaugrund, E., U. Bartsch, R. Martini R, M. Schachner, and M. Schwartz (1990) Immunological evidence that the neural adhesion molecule L1 is expressed in fish brain and optic nerve: Possible association with optic nerve regeneration. Brain Res. 530:239-244.
18. Bixby, J.L., J. Lilien, and L.F. Reichardt (1988) Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J. Cell Biol. 107:353-361.
19. Burrill, J., and S.S. Easter (1994) Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio). J. Comp. Neurol. 346:583-600.
20. Chong, M.S., M.L. Reynolds, N. Irwin, R.E. Coggeshall, P.C. Emson, L. Benowitz, and C.J. Woolf (1994) GAP-43 expression in primary sensory neurons following central axotomy. J. Neurosci. 14:4375-4384.
21. Doherty, P., and F.S. Walsh (1994) Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Curr. Opin. Neurobiol. 4:49-55.
22. Doster, S.K., A.M. Lozano, A.J. Aguayo, and M.B. Willard (1991) Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron 6:635-647.
23. Drazba, J., and V. Lemmon (1990) The role of cell adhesion molecules in neurite outgrowth on Müller cells. Dev. Biol. 138:82-93.
24. Easter, S.S., A.C. Rusoff, and P.E. Kish (1981) The growth and organization of the optic nerve and tract in juvenile and adult goldfish. J. Neurosci. 1:793-811.
25. Erickson, H.P., and M.A. Bourdon (1989) Tenascin: An extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annu. Rev. Cell Biol. 5:71-92.
26. Fawcett, J.W. (1992) Intrinsic neuronal determinants of regeneration. Trends Neurosci. 15:5-8.
27. Gaze, R.M. (1970) The Formation of Nerve Connections. London: Academic Press.
28. Gloor, S., H. Antonicek, K.J. Sweadner, S. Pagliusi, R. Frank, M. Moos, and M. Schachner (1990) The adhesion molecule on glia (AMOG) is a homologue of the beta subunit of the Na,K-ATPase. J. Cell Biol. 110:165-174.
29. Goodman, C.S., and C.J. Shatz (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72:77-98.
30. Jessell, T.M. (1988) Adhesion molecules and the hierarchy of neural development. Neuron 1:3-13.
31. Johns, P.R. (1977) Growth of the adult goldfish eye. III. Source of new retinal cells. J. Comp. Neurol. 176:343-358.
32. Kleitman, N.D., K. Simon, M. Schachner, and R.P. Bunge (1988) Growth of embryonic retinal neurites elicited by contact with Schwann cell surfaces is blocked by antibodies to L1. Exp. Neurol. 102:298-306.
33. Kuhn, T.B., E.T. Stoeckli, M.A. Condrau, F.G. Rathjen, and P. Sonderegger (1991) Neurite outgrowth on immobilized axonin-1 is mediated by heterophilic interaction with L1 (G4). J. Cell Biol. 115:1113-1126.
34. Landmesser, L., L. Dahm, K. Schultz, and U. Rutishauser (1988) Distinct roles for adhesion molecules during the innervation of embryonic chick muscle. Dev. Biol. 130:645-670.
35. Larison, K.D., and R. Bremiller (1990) Early onset of phenotype and cell patterning in the embryonic zebrafish retina. Development 109:567-576.
36. Magyar, J.P., U. Bartsch, Z. Wang, N. Howells, A. Aguzzi, E.F. Wagner, and M. Schachner (1994) Degeneration of neural cells in the central nervous system of mice deficient in the gene for the adhesion molecule on glia, the beta2 subunit of murine Na,K-ATPase. J. Cell Biol. 127:835-845.
37. Martin-Vasallo, P., W. Dackowski, J.R. Emanuel, and R. Levenson (1989) Identification of a putative isoform of the Na,K-ATPase β subunit. J. Biol. Chem. 264:4613-4618.
38. Martini, R. (1994) Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J. Neurocytol. 23:1-28.
39. Martini R., and M. Schachner (1988) Immunelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and myelin-associated glycoprotein) in the regenerating adult mouse sciatic nerve. J. Cell Biol. 106:1735-1746.
40. Meyer, R.L., K. Sakurai, and E. Schauwecker (1985) Topography of regenerating optic fibers in goldfish traced with local wheat germ injections into retina: Evidence for discontinuous microtopography in the retinotectal projection. J. Comp. Neurol. 239:27-43.
41. Mohajeri, M.H., U. Bartsch, H. van der Putten, G. Sansig, L. Mucke, and M. Schachner (1996) Neurite outgrowth on non-permissive substrates in vitro is enhanced by ectopic expression of the neural cell adhesion molecule L1 by mouse astrocytes. Eur. J. Neurosci. 8:1085-1097.
42. Molthagen, M., M. Schachner, and U. Bartsch (1996) Apoptopic cell death of photoreceptor cells in mice deficient for the adhesion molecule on glia (AMOG, the beta2 subunit of the Na,K-ATPase). J Neurocytol. 25:243-255.
43. Müller-Husmann, G., S. Gloor, and M. Schachner (1993) Functional characterization of beta isoforms of murine Na,K-ATPase: The adhesion molecule on glia (AMOG/β2), but not β1, promotes neurite outgrowth. J. Biol. Chem. 263:26260-26267.
44. Pagliusi, S.R., M. Schachner, P.H. Seeburg, and B.D. Shivers (1989) The adhesion molecule on glia (AMOG) is widely espressed by astrocytes in developing and adult mouse brain. Eur. J. Neurosci. 2:471-480.
45. Rathjen, F.G., and T.M. Jessell (1991). Glycoproteins that regulate the growth and guidance of vertebrate axons: Domains and dynamics of the immunoglobulin/fibronectin type III subfamily. Semin. Neurosci. 3:297-307.
46. Reichardt, L.F., and K.J. Tomaselli (1991). Extracellular matrix molecules and their receptors: Functions in neural development. Annu. Rev. Neurosci. 14:531-570.
47. Saga, Y., T. Yagi, Y. Ikawa, T. Sakakura, and S. Aizawa (1992) Mice develop normally without tenascin. Genes and Dev. 6:1821-1831.
48. Schachner, M., S.U. Kim, and R. Zehnle (1981) Developmental expression in central and peripheral nervous system of oligodendroeyte cell surface antigens (O antigens) recognized by monoclonal antibodies. Dev. Biol. 83:328-338.
49. Schachner, M., J. Taylor, U. Bartsch, and P. Pesheva (1994) The perplexing multifunctionality of janusin, a tenascin-related molecule. Persp. Dev. Neurobiol. 2:33-41.
50. Schachner, M., H. Antonicek, T. Fahrig, A. Faissner, G. Fischer G, V. Künemund, R. Martini, A. Meyer, E. Persohn, E. Pollerberg, R. Probstmeier, K. Sadoul, R. Sadoul, B. Seilheimer, and G. Thor (1990) Families of neural cell adhesion molecules. In: G.M. Edelman, B.A. Cunningham and J.P. Thiery (eds): Morphoregulatory Molecules. New York: John Wiley & Sons, pp. 443-468.
51. Schreyer, D.J., and J.H.P. Skene (1991) Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: Delayed accumulation and correlation with regenerative potential. J. Neurosci. 11:3738-3751.
52. Schwab, M.E., J.P. Kapfhammer, and C.E. Bandtlow (1993) Inhibitors of neurite outgrowth. Annu. Rev. Neurosci. 16:565-595.
53. Schwalb, J.M., N.M. Boulis, M. Gu, J. Winickhoff, P.S. Jackson, N. Irwin, and L.I. Benowitz (1995) Two factors secreted by goldfish optic nerveinduce retinal ganglion cells to regenerate axons in culture. J. Neurosci. 15:5514-5525.
54. Seilheimer, B., and M. Schachner (1988) Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture. J. Cell Biol. 107:341-351.
55. Sivron, T., and M. Schwartz (1994) The enigma of myelin-associated growth inhibitors in spontaneously regenerating nervous systems. Trends Neurosci. 17:277-281.
56. Sivron, T., and M. Schwartz (1995) Glial cell types, lineages, and response to injury in rat and fish: Implications for regeneration. Glia 13:157-165.
57. 4) to oligodendrocyte surfaces: An immunocytological study in the central nervous system. Dev. Biol. 83:311-327.
58. Steindler, A.D., D. Settles, H.P. Erickson, E.D. Lavwell, A. Yoshiki, A. Faissner, and M. Kusakabe (1995) Tenascin knockout mice: barrels, boundary molecules, and glial scars. J. Neurosci. 15:1971-1983.
59. Stoeckli, E.T., and L.T. Landmesser (1995) Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14:1165-1179.
60. Stuermer, C.A.O. (1988) Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J. Neurosci. 8:4513-4530.
61. Stuermer, C.A.O., M. Bastmeyer, M. Bähr, G. Strobel, and K. Paschke (1992) Trying to understand axonal regeneration in the CNS of fish. J. Neurobiol 23:537-550.
62. Takeichi, M. (1991). Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251:1451-1455.
63. Tongiorgi, E., R.R. Bernhardt, and M. Schachner (1995a) Zebrafish neurons express two L1-related molecules during axonogensis. J. Neurosci. Res. 4:547-561.
64. Tongiorgi, E., R.R. Bernhardt, K. Zinn, and M. Schachner (1995b) Tenascin-C mRNA is expressed in cranial neural crest cells, in some placodal derivatives, and in discrete domains of the embryonic zebrafish brain. J. Neurobiol. 28:391-407.
65. Tucker, R.P., J.K. Brinso-Bechtold , D.A. Jenrath, N.A. Kahn, P.M. Poss, A.J. Sweatt, and Y. Xu (1994) Cellular origins of tenascin in the developing nervous system. Persp. Dev. Neurobiol. 2:89-99.
66. Vaudano E., G. Campbell, P.N. Anderson, A.P. Davies, C. Woolhead, D.J. Schreyer, and A.R. Lieberman (1995) The effects of a lesion or a peripheral nerve graft on GAP-43 upregulation in the adult rat brain: An in situ hybridization and immunocytochemical study. J. Neurosci. 15:3594-3611.
67. Vielmetter, J., F. Lottspeich, and C.A.O. Stuermer (1991) The monoclonal antibody E587 recognizes growing (new and regenerating) retinal axons in the goldfish retinotectal pathway. J. Neurosci. 11:3581-3593.
68. Wanner, M., D.M. Lang, C.E. Bandtlow, M.E. Schwab, M. Bastmeyer, and C.A.O. Stuermer (1995) Re-evaluation of the growth-permissive substrate properties of goldfish optic nerve myelin and myelin proteins. J. Neurosci. 15:7500-7508.
69. Watts, A.G., G. Sanchez-Watts, J.R. Emanuel, and R. Levenson (1991) Cell-specific expression of mRNAs encoding Na,K-ATPase α- and β-subunit isoforms within the rat central nervous system. Proc. Natl. Acad. Sci. USA 88:7425-7429.
70. Westerfield, M. (1993) The Zebrafish Book. Eugene, OR: University of Oregon Press.
71. Zhang, Y., G. Campbell, P.N. Anderson, R. Martini, M. Schachner, and R. Lieberman (1995) Molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts. I. Neural cell adhesion molecules. J. Comp. Neurol. 361:193-209.